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Transcription establishes microenvironments that organize euchromatin

View ORCID ProfileLennart Hilbert, Yuko Sato, View ORCID ProfileHiroshi Kimura, View ORCID ProfileFrank Jülicher, View ORCID ProfileAlf Honigmann, Vasily Zaburdaev, View ORCID ProfileNadine Vastenhouw
doi: https://doi.org/10.1101/234112
Lennart Hilbert
1Center for Systems Biology Dresden, 01307 Dresden, Germany;
2Max Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany;
3Max Planck Institute for the Physics of Complex Systems, 01187 Dresden, Germany;
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Yuko Sato
4Tokyo Institute of Technology, 226-8503 Yokohama, Kanagawa, Japan;
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Hiroshi Kimura
4Tokyo Institute of Technology, 226-8503 Yokohama, Kanagawa, Japan;
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Frank Jülicher
1Center for Systems Biology Dresden, 01307 Dresden, Germany;
3Max Planck Institute for the Physics of Complex Systems, 01187 Dresden, Germany;
5Center for Advancing Electronics Dresden, Technical University Dresden, 01062 Dresden;
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Alf Honigmann
2Max Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany;
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Vasily Zaburdaev
1Center for Systems Biology Dresden, 01307 Dresden, Germany;
3Max Planck Institute for the Physics of Complex Systems, 01187 Dresden, Germany;
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Nadine Vastenhouw
2Max Planck Institute of Molecular Cell Biology and Genetics, 01307 Dresden, Germany;
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  • ORCID record for Nadine Vastenhouw
  • For correspondence: vastenhouw@mpi-cbg.de
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Abstract

Summary The three-dimensional organization of the genome is essential for development and health. Although the organization of euchromatin (transcriptionally permissive chromatin) dynamically adjusts to changes in transcription, the underlying mechanisms remain elusive. Here, we studied how transcription organizes euchromatin, using experiments in zebrafish embryonic cells and theory. We show that transcription establishes an interspersed pattern of chromatin domains and RNA-enriched microenvironments. Specifically, accumulation of RNA in the vicinity of transcription sites creates microenvironments that locally remodel chromatin by displacing not transcribed chromatin. Ongoing transcriptional activity stabilizes the interspersed pattern of chromatin domains and RNA-enriched microenvironments by establishing contacts between chromatin and RNA. We explain our observations with an active microemulsion model based on two macromolecular mechanisms: RNA/RNA-binding protein complexes generally segregate from chromatin, while transcribed chromatin is retained among RNA/RNA-binding protein accumulations. We propose that microenvironments might be central to genome architecture and serve as gene regulatory hubs.

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Highlights

  • Transcription establishes microenvironments that remodel euchromatin

  • Microenvironments form by RNA accumulation in the vicinity of transcription sites

  • Microenvironments exclude not transcribed DNA and retain transcribed DNA

  • Euchromatin is organized like an active microemulsion, stabilized by transcription

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted December 15, 2017.
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Transcription establishes microenvironments that organize euchromatin
Lennart Hilbert, Yuko Sato, Hiroshi Kimura, Frank Jülicher, Alf Honigmann, Vasily Zaburdaev, Nadine Vastenhouw
bioRxiv 234112; doi: https://doi.org/10.1101/234112
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Transcription establishes microenvironments that organize euchromatin
Lennart Hilbert, Yuko Sato, Hiroshi Kimura, Frank Jülicher, Alf Honigmann, Vasily Zaburdaev, Nadine Vastenhouw
bioRxiv 234112; doi: https://doi.org/10.1101/234112

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